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A cell-type-specific alternative splicing regulator shapes synapse properties in a trans-synaptic manner

Traunmüller, Lisa, Schulz, Jan, Ortiz, Raul, Feng, Huijuan, Furlanis, Elisabetta, Gomez, Andrea M., Schreiner, Dietmar, Bischofberger, Josef, Zhang, Chaolin, Scheiffele, Peter·2023·Cell Reports
DOI 10.1016/j.celrep.2023.112173PMC PMC10066595
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Figure 1 SLM2-bound mRNAs encode synaptic proteins (A) Endogenous SLM2 immunoreactivity (green) and DAPI (purple) in hippocampus. Scale bar, 1 μm. (B) Immunostaining for SLM2 (green) and SAM68 (magenta) in cultured hippocampal neurons (day in vitro 12). Insets show enlargement of boxed area. Scale bar, 1 μm. (C) Cluster annotation summary for input and eCLIP samples. (D) Enrichment of UWAA around cross-link-induced truncation site (CITS), calculated from frequency of UWAA starting at each position relative to the inferred cross-link sites, normalized by frequency of the element in flanking sequences in whole-brain eCLIP data. Enrichment of UWAA around the CLIP tag cluster peak center shown for comparison. (E) SLM2 binding motif determined by mCross in whole-brain eCLIP data. Cross-linking frequencies at each motif position represented by blue bars. (F) Number of high-confidence SLM2 targets identified by CLIPper and IDR analysis (log2 fold change ≥ 2 and −log10(IDR) ≥ 2) in whole-brain and hippocampal eCLIP samples. (G) Gene Ontology analysis (DAVID tools) of genes with significant SLM2 binding sites (whole brain). Top 10 enriched Gene Ontology categories for cellular compartment displayed. (H) Sunburst chart and gene examples associated with synaptic function of high-confidence eCLIP targets from whole-brain samples identified by CLIPper and IDR. (I) SLM2 eCLIP read densities on eCLIP targets compared with size-matched input. UWAA motif enrichment in whole-brain (green) and hippocampal (orange) samples. Coordinates shown are Grm5 chr7: 87,601,936–87,607,378 and Cadm1 chr9: 47,836,291–47,840,954.
Figure 1 SLM2-bound mRNAs encode synaptic proteins (A) Endogenous SLM2 immunoreactivity (green) and DAPI (purple) in hippocampus. Scale bar, 1 μm. (B) Immunostaining for SLM2 (green) and SAM68 (magenta) in cultured hippocampal neurons (day in vitro 12). Insets show enlargement of boxed area. Scale bar, 1 μm. (C) Cluster annotation summary for input and eCLIP samples. (D) Enrichment of UWAA around cross-link-induced truncation site (CITS), calculated from frequency of UWAA starting at each position relative to the inferred cross-link sites, normalized by frequency of the element in flanking sequences in whole-brain eCLIP data. Enrichment of UWAA around the CLIP tag cluster peak center shown for comparison. (E) SLM2 binding motif determined by mCross in whole-brain eCLIP data. Cross-linking frequencies at each motif position represented by blue bars. (F) Number of high-confidence SLM2 targets identified by CLIPper and IDR analysis (log2 fold change ≥ 2 and −log10(IDR) ≥ 2) in whole-brain and hippocampal eCLIP samples. (G) Gene Ontology analysis (DAVID tools) of genes with significant SLM2 binding sites (whole brain). Top 10 enriched Gene Ontology categories for cellular compartment displayed. (H) Sunburst chart and gene examples associated with synaptic function of high-confidence eCLIP targets from whole-brain samples identified by CLIPper and IDR. (I) SLM2 eCLIP read densities on eCLIP targets compared with size-matched input. UWAA motif enrichment in whole-brain (green) and hippocampal (orange) samples. Coordinates shown are Grm5 chr7: 87,601,936–87,607,378 and Cadm1 chr9: 47,836,291–47,840,954.CC BY · PubMed Central
Figure 2 Conditional ablation of SLM2 in hippocampal cell types (A) Cre drivers to assess the molecular profile of hippocampal Cornu Ammonis (CA) 1 (CamK2-cre), CA3 (Grik4-cre), and SST-positive (SST-cre) neurons. (B) Fitted Gaussian curves of relative frequency of SLM2 immunoreactivity in CA1, CA3 and SST cre-positive neurons in the stratum oriens (s.o) of CA1 and CA3. Background immunoreactivity defined based on staining of global Slm2KO mice. n = 3 animals each. CA1: 68 cells, CA3: 75 cells, SST CA1 s.o: 73 cells, SST CA3 s.o: 60 cells, dentate gyrus (DG): 62 cells. (C) SLM2 expression in cre-positive cells defined by immunoreactivity for conditional Rpl22HA allele in Slm2+/+ and Slm2fl/fl mice (HA: magenta, SLM2: green, scale bar, 40 μm). (D) Quantification of SLM2 deletion efficiency at P42–45 in CA1 (ΔCamK2, N = 4, n = 1,081) and CA3 (ΔGrik4, N = 4, n = 1,070) and at P16–18 in SST (ΔSST, N = 5, n = 157) neurons. Mean ± SEM. (E) Principal-component analysis of genes expressed in hippocampal Slm2 wild-type and conditional knockout RiboTRAP pull-downs (wild type [WT] in green: Grik4cre:Rpl22HA/HA N = 4, ΔGrik4: Grik4cre::Rpl22HA/HA::Slm2fl/fl N = 4; WT in purple: Camk2cre::Rpl22HA/HA N = 3, ΔCamK2: Camk2cre::Rpl22HA/HA::Slm2fl/fl N = 3; WT in red: SSTcre::Rpl22HA/HA N = 4, ΔSST: SSTcre::Rpl22HA/HA::Slm2fl/fl N = 4). Variances explained by principal component 1 (PC1) and PC2 are indicated. Variance stabilization transformation was utilized to normalize gene expression. (F) Correlation analysis of the mean log10 transformed, normalized transcript counts (reads per kilobase million [rpkm]) between WT (x axis) and mutants (y axis). Differentially expressed genes (fold change ≥ 1.5, adjusted p value Benjamini and Hochberg ≤ 0.05) are marked in color.
Figure 2 Conditional ablation of SLM2 in hippocampal cell types (A) Cre drivers to assess the molecular profile of hippocampal Cornu Ammonis (CA) 1 (CamK2-cre), CA3 (Grik4-cre), and SST-positive (SST-cre) neurons. (B) Fitted Gaussian curves of relative frequency of SLM2 immunoreactivity in CA1, CA3 and SST cre-positive neurons in the stratum oriens (s.o) of CA1 and CA3. Background immunoreactivity defined based on staining of global Slm2KO mice. n = 3 animals each. CA1: 68 cells, CA3: 75 cells, SST CA1 s.o: 73 cells, SST CA3 s.o: 60 cells, dentate gyrus (DG): 62 cells. (C) SLM2 expression in cre-positive cells defined by immunoreactivity for conditional Rpl22HA allele in Slm2+/+ and Slm2fl/fl mice (HA: magenta, SLM2: green, scale bar, 40 μm). (D) Quantification of SLM2 deletion efficiency at P42–45 in CA1 (ΔCamK2, N = 4, n = 1,081) and CA3 (ΔGrik4, N = 4, n = 1,070) and at P16–18 in SST (ΔSST, N = 5, n = 157) neurons. Mean ± SEM. (E) Principal-component analysis of genes expressed in hippocampal Slm2 wild-type and conditional knockout RiboTRAP pull-downs (wild type [WT] in green: Grik4cre:Rpl22HA/HA N = 4, ΔGrik4: Grik4cre::Rpl22HA/HA::Slm2fl/fl N = 4; WT in purple: Camk2cre::Rpl22HA/HA N = 3, ΔCamK2: Camk2cre::Rpl22HA/HA::Slm2fl/fl N = 3; WT in red: SSTcre::Rpl22HA/HA N = 4, ΔSST: SSTcre::Rpl22HA/HA::Slm2fl/fl N = 4). Variances explained by principal component 1 (PC1) and PC2 are indicated. Variance stabilization transformation was utilized to normalize gene expression. (F) Correlation analysis of the mean log10 transformed, normalized transcript counts (reads per kilobase million [rpkm]) between WT (x axis) and mutants (y axis). Differentially expressed genes (fold change ≥ 1.5, adjusted p value Benjamini and Hochberg ≤ 0.05) are marked in color.CC BY · PubMed Central
Figure 3 SLM2 directly regulates alternative splicing of mRNAs encoding synaptic proteins (A) Log2 fold change splicing index (FC SI) and −log10 p values of splicing patterns comparing WT and Slm2 mutants. Significantly regulated exons are marked in color (fold change ≥ 2, p ≤ 0.01). (B and C) Sequencing tracks for WT and mutant (Δ) RiboTrap samples for hippocampal Grik4, CamK2, and SST cells and eCLIP analysis in whole brain and hippocampus for de-regulated exons of Nrxn2 and Nrxn3. SLM2 binding events in downstream introns align with UWAA motifs. Coordinates: Nrxn2 chr19:6,509,778–6,517,248; Nrxn3 chr12:90,168,920–90,204,818.
Figure 3 SLM2 directly regulates alternative splicing of mRNAs encoding synaptic proteins (A) Log2 fold change splicing index (FC SI) and −log10 p values of splicing patterns comparing WT and Slm2 mutants. Significantly regulated exons are marked in color (fold change ≥ 2, p ≤ 0.01). (B and C) Sequencing tracks for WT and mutant (Δ) RiboTrap samples for hippocampal Grik4, CamK2, and SST cells and eCLIP analysis in whole brain and hippocampus for de-regulated exons of Nrxn2 and Nrxn3. SLM2 binding events in downstream introns align with UWAA motifs. Coordinates: Nrxn2 chr19:6,509,778–6,517,248; Nrxn3 chr12:90,168,920–90,204,818.CC BY · PubMed Central
Figure 4 SLM2 controls synaptic plasticity and function in a trans-synaptic manner (A) Electrical stimulation of axons in the alveus and voltage-clamp recordings in genetically marked SST-positive interneurons in the s.o. (B) Example traces of miniature excitatory postsynaptic currents (mEPSCs) in SST interneurons. (C–E) Analysis of mEPSC amplitude (C), frequency (D), and rise and decay times (E). WT n = 17, ΔSST n = 18. Mean ± SEM. p values determined by corresponding t tests. For cumulative frequency distribution, Kolmogorov-Smirnov test. (F) Mean ± SEM data of AMPAR-mediated EPSCs in SST interneurons of s.o in response to different stimulation intensities of axons in the alveus in ΔSST n = 17 versus WT n = 12. Two-way ANOVA with Šídák’s multiple comparisons test. (G) Representative traces of evoked EPSCs during repetitive stimulation at 40 Hz in WT (black) and ΔSST (red). Group data of EPSCs normalized to the first peak in ΔSST n = 26 versus WT n = 26. Mean ± SEM. Two-way ANOVA with Šídák’s multiple comparisons test. (H) Local optogenetic stimulation of SST+ neuron-mediated IPSCs in apical CA1 dendrites in WT and ΔSST mutants. Representative traces of inward and outward IPSCs evoked at increasing laser intensities in WT (black) and ΔSST (red). Mean ± SEM input-output curve of synaptic conductance underlying outward and inward PSCs. (I) Quantification of velocity (cm/min) in open field, initial, and short-term memory (STM) test phases of novel object recognition (NOR) task. Animal numbers for each task are indicated. Mean ± SEM, unpaired t test. (J and K) NOR interaction time (s) spent with a familiar (black) or novel (purple) object during a 5 min trial (paired t test) and discrimination index (unpaired t test). Mean ± SEM, WT n = 19 and ΔSST n = 12.
Figure 4 SLM2 controls synaptic plasticity and function in a trans-synaptic manner (A) Electrical stimulation of axons in the alveus and voltage-clamp recordings in genetically marked SST-positive interneurons in the s.o. (B) Example traces of miniature excitatory postsynaptic currents (mEPSCs) in SST interneurons. (C–E) Analysis of mEPSC amplitude (C), frequency (D), and rise and decay times (E). WT n = 17, ΔSST n = 18. Mean ± SEM. p values determined by corresponding t tests. For cumulative frequency distribution, Kolmogorov-Smirnov test. (F) Mean ± SEM data of AMPAR-mediated EPSCs in SST interneurons of s.o in response to different stimulation intensities of axons in the alveus in ΔSST n = 17 versus WT n = 12. Two-way ANOVA with Šídák’s multiple comparisons test. (G) Representative traces of evoked EPSCs during repetitive stimulation at 40 Hz in WT (black) and ΔSST (red). Group data of EPSCs normalized to the first peak in ΔSST n = 26 versus WT n = 26. Mean ± SEM. Two-way ANOVA with Šídák’s multiple comparisons test. (H) Local optogenetic stimulation of SST+ neuron-mediated IPSCs in apical CA1 dendrites in WT and ΔSST mutants. Representative traces of inward and outward IPSCs evoked at increasing laser intensities in WT (black) and ΔSST (red). Mean ± SEM input-output curve of synaptic conductance underlying outward and inward PSCs. (I) Quantification of velocity (cm/min) in open field, initial, and short-term memory (STM) test phases of novel object recognition (NOR) task. Animal numbers for each task are indicated. Mean ± SEM, unpaired t test. (J and K) NOR interaction time (s) spent with a familiar (black) or novel (purple) object during a 5 min trial (paired t test) and discrimination index (unpaired t test). Mean ± SEM, WT n = 19 and ΔSST n = 12.CC BY · PubMed Central

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Metadata

Authors
Traunmüller, L., Schulz, J., Ortiz, R., Feng, H., Furlanis, E., Gomez, A. M., Schreiner, D., Bischofberger, J., Zhang, C., & Scheiffele, P.
Venue
Cell Reports
Publisher
Elsevier BV
Published
2023-03
Volume
42
Issue
3
Pages
112173
ISSN
2211-1247
DOI
10.1016/j.celrep.2023.112173
PMC
PMC10066595
Cited by
31
References
14
Language
en
Licence
Funders
  • National Institutes of Health (R01NS125018)
  • European Research Council (AIMS-2-TRIALS)
  • Schweizerischer Nationalfonds zur Förderung der Wissenschaftlichen Forschung (179432, TMAG-3-209273, 176321)
  • European Commission
  • Universität Basel

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Data sources

Bibliographic data: Semantic Scholar, OpenAlex, Crossref.

Contains information from the Semantic Scholar Academic Graph Datasets, made available under the ODC Attribution License (ODC-BY 1.0).

Semantic Scholar’s data is described in: Kinney, R., et al. (2023). The Semantic Scholar Open Data Platform. arXiv:2301.10140.